Saponins from Panax japonicus attenuate cognitive impairment in ageing rats through regulating microglial polarisation and autophagy

References

• Belarbi K, Rosi S. 2013. Modulation of adult-born neurons in the inflamed hippocampus. Front Cell Neurosci. 7:145–153.
   PubMed Web of Science ®Google Scholar
• Block ML, Zecca L, Hong JS. 2007. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci. 8(1):57–69.
   PubMed Web of Science ®Google Scholar
• Bussi C, Peralta RJ, Arroyo DS, Gaviglio EA, Gallea JI, Wang JM, Celej MS, Iribarren P. 2017. Autophagy down regulates pro-inflammatory mediators in BV2 microglial cells and rescues both LPS and alpha-synuclein induced neuronal cell death. Sci Rep. 7:43153–43161.
   PubMed Web of Science ®Google Scholar
• Cadwell K. 2016. Crosstalk between autophagy and inflammatory signalling pathways: balancing defence and homeostasis. Nat Rev Immunol. 16(11):661–675.
   PubMed Web of Science ®Google Scholar
• Carneiro LA, Travassos LH. 2013. The interplay between NLRs and autophagy in immunity and inflammation. Front Immunol. 4:361–374.
   PubMed Web of Science ®Google Scholar
• Cheng J, Liao Y, Dong Y, Hu H, Yang N, Kong X, Li S, Li X, Guo J, Qin L, et al. 2020. Microglial autophagy defect causes Parkinson disease-like symptoms by accelerating inflammasome activation in mice. Autophagy. 16(12):2193–2205.
   PubMed Web of Science ®Google Scholar
• Colonna M, Butovsky O. 2017. Microglia function in the central nervous system during health and neurodegeneration. Annu Rev Immunol. 35:441–468.
   PubMed Web of Science ®Google Scholar
• Dai YW, Yuan D, Wan JZ, Zhang CC, Liu CQ, Wang T. 2014. Study on protective effect of total saponins of Panax japonicus on LPS-induced RAW264.7 cell inflammation through NF-κB pathway. Chin J Chin Mater Med. 39:2076–2080.
   Google Scholar
• de Mattos Barbosa MG, de Andrade Silva BJ, Assis TQ, da Silva Prata RB, Ferreira H, Andrade PR, da Paixão de Oliveira JA, Sperandio da Silva GM, da Costa Nery JA, Sarno EN, Pinheiro RO. 2018. Autophagy impairment is associated with increased inflammasome activation and reversal reaction development in multibacillary leprosy. Front Immunol. 9:1223–1234.
   PubMed Web of Science ®Google Scholar
• Deng LL, Yuan D, Zhou ZY, Wan JZ, Zhang CC, Liu CQ, Dun YY, Zhao HX, Zhao B, Yang YJ, et al. 2017. Saponins from Panax japonicus attenuate age-related neuroinflammation via regulation of the mitogen-activated protein kinase and nuclear factor kappa B signaling pathways. Neural Regen Res. 12(11):1877–1884.
   PubMed Web of Science ®Google Scholar
• Fan LW, Pang Y. 2017. Dysregulation of neurogenesis by neuroinflammation: key differences in neurodevelopmental and neurological disorders. Neural Regen Res. 12(3):366–371.
   PubMed Web of Science ®Google Scholar
• Ferrucci L, Corsi A, Lauretani F, Bandinelli S, Bartali B, Taub DD, Guralnik JM, Longo DL. 2005. The origins of age-related proinflammatory state. Blood. 105(6):2294–2299.
   PubMed Web of Science ®Google Scholar
• Gammon K. 2014. Neurodegenerative disease: brain windfall. Nature. 515(7526):299–300.
   PubMedGoogle Scholar
• Goldberg EL, Dixit VD. 2015. Drivers of age-related inflammation and strategies for healthspan extension. Immunol Rev. 265(1):63–74.
   PubMed Web of Science ®Google Scholar
• Guo H, Callaway JB, Ting JP. 2015. Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat Med. 21(7):677–687.
   PubMed Web of Science ®Google Scholar
• Han X, Sun S, Sun Y, Song Q, Zhu J, Song N, Chen M, Sun T, Xia M, Ding J, et al. 2019. Small molecule-driven NLRP3 inflammation inhibition via interplay between ubiquitination and autophagy: implications for Parkinson disease. Autophagy. 15(11):1860–1881.
   PubMed Web of Science ®Google Scholar
• He C, Yu Z, He Y, Xu C, Chang C, Yuan D. 2017. Purification of macroporous adsorption resin and decolorization of ion exchange resin of total saponins of Panax japonicus. Chia Tradit Herbal Drugs. 48:1146–1152.
   Google Scholar
• He Y, She H, Zhang T, Xu H, Cheng L, Yepes M, Zhao Y, Mao Z. 2018. p38 MAPK inhibits autophagy and promotes microglial inflammatory responses by phosphorylating ULK1. J Cell Biol. 217(1):315–328.
   PubMed Web of Science ®Google Scholar
• Houtman J, Freitag K, Gimber N, Schmoranzer J, Heppner FL, Jendrach M, 2019. Beclin1-driven autophagy modulates the inflammatory response of microglia via NLRP3. Embo J. 38(4):38–49. 4.
   Web of Science ®Google Scholar
• Hu X, Leak RK, Shi Y, Suenaga J, Gao Y, Zheng P, Chen J. 2015. Microglial and macrophage polarization—new prospects for brain repair . Nat Rev Neurol. 11(1):56–64.
   PubMed Web of Science ®Google Scholar
• Jin MM, Wang F, Qi D, Liu WW, Gu C, Mao CJ, Yang YP, Zhao Z, Hu LF, Liu CF. 2018. A critical role of autophagy in regulating microglia polarization in neurodegeneration. Front Aging Neurosci. 10:378–389.
   PubMed Web of Science ®Google Scholar
• Kim JY, Paton JC, Briles DE, Rhee DK, Pyo S. 2015. Streptococcus pneumoniae induces pyroptosis through the regulation of autophagy in murine microglia. Oncotarget. 6(42):44161–44178.
   PubMedGoogle Scholar
• Lee JW, Nam H, Kim LE, Jeon Y, Min H, Ha S, Lee Y, Kim SY, Lee SJ, Kim EK, et al. 2019. TLR4 (toll-like receptor 4) activation suppresses autophagy through inhibition of FOXO3 and impairs phagocytic capacity of microglia. Autophagy. 15(5):753–770.
   PubMed Web of Science ®Google Scholar
• Li D, Wang C, Yao Y, Chen L, Liu G, Zhang R, Liu Q, Shi FD, Hao J. 2016. mTORC1 pathway disruption ameliorates brain inflammation following stroke via a shift in microglia phenotype from M1 type to M2 type. Faseb J. 30(10):3388–3399.
   PubMed Web of Science ®Google Scholar
• Lutshumba J, Nikolajczyk BS, Bachstetter AD. 2021. Dysregulation of systemic immunity in aging and dementia. Front Cell Neurosci. 15:652111–652158.
   PubMed Web of Science ®Google Scholar
• Miron VE, Boyd A, Zhao J-W, Yuen TJ, Ruckh JM, Shadrach JL, van Wijngaarden P, Wagers AJ, Williams A, Franklin RJM, et al. 2013. M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination. Nat Neurosci. 16(9):1211–1218.
   PubMed Web of Science ®Google Scholar
• Munz C. 2016. Autophagy beyond intracellular MHC Class II antigen presentation. Trends Immunol. 37:755–763.
   PubMed Web of Science ®Google Scholar
• Nilsson CJ, Nørgaard S, Foverskov E, Bruunsgaard H, Andersen PK, Lund R. 2020. Positive and negative aspects of social relations and low-grade inflammation in Copenhagen Aging and Midlife Biobank. Eur J Ageing. 17(4):531–546.
   PubMed Web of Science ®Google Scholar
• Prinz M, Priller J. 2014. Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease. Nat Rev Neurosci. 15(5):300–312.
   PubMed Web of Science ®Google Scholar
• Ruan B, Wang R, Yang YJ, Wang DF, Wang JW, Zhang CC, Yuan D, Zhou ZY, Wang T. 2019. Improved effects of saponins from Panax japonicus on decline of cognitive function in natural aging rats via NLRP3 inflammasome pathway. Chin J Chin Mater Med. 44:344–349. Chinese
   Google Scholar
• Saitoh T, Akira S. 2010. Regulation of innate immune responses by autophagy-related proteins. J Cell Biol. 189(6):925–935.
   PubMed Web of Science ®Google Scholar
• Saxena S, Kruys V, Vamecq J, Maze M. 2021. The role of microglia in perioperative neuroinflammation and neurocognitive disorders. Front Aging Neurosci. 13:671499–671534.
   PubMed Web of Science ®Google Scholar
• Smith JA, Das A, Ray SK, Banik NL. 2012. Role of pro-inflammatory cytokines released from microglia in neurodegenerative diseases. Brain Res Bull. 87(1):10–20.
   PubMed Web of Science ®Google Scholar
• Su P, Zhang J, Wang D, Zhao F, Cao Z, Aschner M, Luo W. 2016. The role of autophagy in modulation of neuroinflammation in microglia. Neuroscience. 319:155–167.
   PubMed Web of Science ®Google Scholar
• Sumpter RJ, Levine B. 2010. Autophagy and innate immunity: triggering, targeting and tuning. Semin Cell Dev Biol. 21(7):699–711.
   PubMed Web of Science ®Google Scholar
• Tian DS, Li CY, Qin C, Murugan M, Wu LJ, Liu JL. 2016. Deficiency in the voltage-gated proton channel Hv1 increases M2 polarization of microglia and attenuates brain damage from photothrombotic ischemic stroke. J Neurochem. 139(1):96–105.
   PubMed Web of Science ®Google Scholar
• Tricco AC, Soobiah C, Lillie E, Perrier L, Chen MH, Hemmelgarn B, Majumdar SR, Straus SE. 2012. Use of cognitive enhancers for mild cognitive impairment: protocol for a systematic review and network meta-analysis. Syst Rev. 1:25–34.
   PubMedGoogle Scholar
• Tu H, Zhou Q, Zhang X, Wang T, Yuan CF, Zhang CC, Yuan D, Liu ZQ. 2018. Protective effects of total saponins of Panax japonicas on HepG2 cell apoptosis induced with palmitic acid. Chin J Chin Mater Med. 43:390–395.
   Google Scholar
• Wan JZ, Wang R, Zhou ZZ, Deng LL, Zhang CC, Liu CQ, Zhao HX, Yuan CF, He YM, Dun YY, Yuan D, et al. 2020. Saponins of Panax japonicus confer neuroprotection against brain aging through mitochondria related oxidative stress and autophagy in rats. Curr Pharm Biotechnol. 21:1–14.
   Web of Science ®Google Scholar
• Wang H, Shen Y, Chuang H, Chiu C, Ye Y, Zhao L. 2019. Neuroinflammation in Alzheimer’s disease: microglia, molecular participants and therapeutic choices. Curr Alzheimer Res. 16(7):659–674.
   PubMed Web of Science ®Google Scholar
• Wang T, Di G, Yang L, Dun Y, Sun Z, Wan J, Peng B, Liu C, Xiong G, Zhang C, et al. 2015. Saponins from Panax japonicus attenuate d-galactose-induced cognitive impairment through its anti-oxidative and anti-apoptotic effects in rats. J Pharm Pharmacol. 67(9):1284–1296.
   PubMed Web of Science ®Google Scholar
• Więckowska-Gacek A, Mietelska-Porowska A, Wydrych M, Wojda U. 2021. Western diet as a trigger of Alzheimer’s disease: from metabolic syndrome and systemic inflammation to neuroinflammation and neurodegeneration. Ageing Res Rev. 21:1568–1637.
   Google Scholar
• Wu QS, Chen P, Zhang QW. 2016. Research progress on chemical constituents, pharmacological activities and analytical methods of Panax japonicus. Asia-Pacific Trad Med. 12:46–54.
   Google Scholar
• Xia CY, Zhang S, Chu SF, Wang ZZ, Song XY, Zuo W, Gao Y, Yang PF, Chen NH. 2016. Autophagic flux regulates microglial phenotype according to the time of oxygen-glucose deprivation/reperfusion. Int Immunopharmacol. 39:140–148.
   PubMed Web of Science ®Google Scholar
• Ye J, Jiang Z, Chen X, Liu M, Li J, Liu N. 2017. The role of autophagy in pro-inflammatory responses of microglia activation via mitochondrial reactive oxygen species in vitro. J Neurochem. 142(2):215–230.
   PubMed Web of Science ®Google Scholar
• Ye X, Zhu M, Che X, Wang H, Liang XJ, Wu C, Xue X, Yang J. 2020. Lipopolysaccharide induces neuroinflammation in microglia by activating the MTOR pathway and downregulating Vps34 to inhibit autophagosome formation. J Neuroinflammation. 17(1):18.
   PubMed Web of Science ®Google Scholar
• Yuan D, Xiang T, Huo Y, Liu C, Wang T, Zhou Z, Dun Y, Zhao H, Zhang C. 2018. Preventive effects of total saponins of Panax japonicus on fatty liver fibrosis in mice. Arch Med Sci. 14(2):396–406.
   PubMed Web of Science ®Google Scholar
• Zhang G, Li J, Purkayastha S, Tang Y, Zhang H, Yin Y, Li B, Liu G, Cai D. 2013. Hypothalamic programming of systemic ageing involving IKK-β, NF-κB and GnRH . Nature. 497(7448):211–216.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Kim MS, Jia B, Yan J, Zuniga-Hertz JP, Han C, Cai D. 2017. Hypothalamic stem cells control ageing speed partly through exosomal miRNAs. Nature. 548(7665):52–57.
   PubMed Web of Science ®Google Scholar
• Zhou X, Zhou J, Li X, Guo C, Fang T, Chen Z. 2011. GSK-3β inhibitors suppressed neuroinflammation in rat cortex by activating autophagy in ischemic brain injury. Biochem Biophys Res Commun. 411:271–275.
   PubMed Web of Science ®Google Scholar
• Zia A, Pourbagher-Shahri AM, Farkhondeh T, Samarghandian S. 2021. Molecular and cellular pathways contributing to brain aging. Behav Brain Funct. 17(1):6–36.
   PubMed Web of Science ®Google Scholar